Abstract
The tubular ray flower (turf) mutant of sunflower is characterized by a switch of ray flowers from zygomorphic to near-actinomorphic disc flowers. In sunflower, floral symmetry of ray and disc flowers is specified by the activity of members of a CYCLOIDEA (CYC) gene family. The turf mutant is generated by the insertion of a CACTA-like transposable element (TE), named Transposable element of turf1 (Tetu1), in the coding sequence of the HaCYC2c gene. The TEinsertion changes the reading frame of turf-HaCYC2c for the encoded protein and leads to a premature stop codon. Tetu1 is a non-autonomous version of a CACTA TEcarrying the minimum sequences necessary for transposition in the presence of autonomous elements in the sunflower genome. In the previous analysis, performed in more than 11 000 plants homozygous for the turf-HaCYC2c allele, the absence of chimerism and the segregation rate of derived-progenies from reverted phenotypes suggest that Tetu1 transpositions are restricted to a time shortly before and/or during meiosis. Here, we report the analysis of F5 and F6 progenies, derived from an F4 progeny of the cross turf × Chrysanthemoides2, where plants with a chimeric inflorescence were detected. Tetu1 showed active excision in all progenies taken into consideration and named High Frequency of Tetu1 Transposition (HFTT). Within a total of 449 plants, Tetu1 excision generated a 13.81 % of non-chimeric revertants but also a 5.12 % of plants with somatic sectors of variable size in the outmost whorl of the inflorescence. These unexpected results suggest variations in tissue specificity and time of TEexcision. The excision of Tetu1 was confirmed by DNA molecular screening of non-chimeric and chimeric revertants and transcription analysis of the HaCYC2c gene. In HFTT progenies, sequence analyses excluded significant DNA changes with respect to the original Tetu1 transposon as well as to the adjacent 5’- and 3’-TE regions. Genetic and epigenetic regulatory mechanisms were proposed to explain the time and frequency of Tetu1 transposition in HFTT progenies.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- Chry2:
-
Chrysanthemoides2
- CpG:
-
5’-Cytosine-phosphate-Guanine-3’
- CYC :
-
CYCLOIDEA
- HFTT:
-
High Frequency of Tetu1 Transposition
- ORF:
-
open reading frame
- RF:
-
ray flowers
- TB1:
-
CYC/TEOSINTE BRANCHED1
- TCP:
-
TEOSINTE-BRANCHED1/CYCLOIDEA/PROLIFE-RATING CELL NUCLEAR ANTIGEN FACTOR1,2
- TE:
-
transposable element
- Tetu1 :
-
Transposable element of turf1
- TIR:
-
terminal inverted repeat
- turf :
-
tubular ray flower
- WT:
-
wild type
References
Alleman, M., Freeling, M.: The Mu transposable element of maize: evidence for transposition and copy number regulation during development. - Genetics 112: 107–119, 1986.
Bennetzen, J.L.: Transposable elements, gene creation and genome rearrangement in flowering plants. - Curr Opin. Genet. Dev. 15: 621–627, 2005.
Berti, F., Fambrini, M., Turi, M., Bertini, D., Pugliesi. C.: Mutations of corolla symmetry affect carpel and stamen development in Helianthus annuus. - Can. J. Bot. 83: 1065–1072, 2005.
Broholm, S.K., Tä htiharju, S., Laitinen, R.A.E., Albert, V.A., Teeri, T.H., Elomaa, P.: A TCP domain transcription factor controls flower type specification along the radial axis of the Gerbera (Asteraceae) inflorescence. - Proc. nat. Acad. Sci. USA 105: 9117–9122, 2008.
Brutnell, T.P., Dellaporta S.L.: Somatic inactivation and reactivation of Ac associated with changes in cytosine methylation and transposase expression. - Genetics 138: 213–225, 1994.
Buchmann, J.P., Lö ytynoja, A., Wicker, T., Schulman, A.H.: Analysis of CACTA transposases reveals intron loss a major factor influencing their exon/intron structure in monocotyledonous and eudicotyledonous hosts. - Mobile DNA 5: 24, 2014.
Busch, A., Zachgo, S.: Flower symmetry evolution: towards understanding the abominable mystery of angiosperm radiation. - BioEssays 31: 1181–1190, 2009.
Calvi, B.R., Hong, T.J., Findley, S.D., Gelbart, W.M.: Evidence for a common evolutionary origin of inverted repeat transposons in Drosophila and plants: hobo, Activator, and Tam3. - Cell 66: 465–471, 1991.
Carlson, S.E., Howard, D.G., Donoghue, M.J.: Diversification of CYCLOIDEA-like genes in Dipsacaceae (Dipsacales): implications for the evolution of capitulum inflorescences. - BMC Evol. Biol. 11: 325, 2011.
Carpenter, R., Coen, E.S.: Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. - Genes Dev. 4: 1483–1493, 1990.
Cavallini, A., Natali, L., Zuccolo, A., Giordani, T., Jurman, I., Ferrillo, V., Vitacolonna, N., Sarri, V., Cattonaro, F., Ceccarelli, M., Cionini, P.G., Morgante, M.: Analysis of transposons and repeat composition of the sunflower (Helianthus annuus L.) genome. - Theor. appl. Genet. 120: 491–508, 2010.
Çetinbas, A., Ünal, M.: Comparative ontogeny of hermaphrodite and pistillate florets in Helianthus annuus L. (Asteraceae). - Not. Sci. Biol. 4: 30–40, 2012.
Chapman, M.A., Leebens-Mack, J.H., Burke, J.M.: Positive selection and expression divergence following gene duplication in the sunflower CYCLOIDEA gene family. - Mol. Biol. Evol. 25: 1260–1273, 2008.
Chapman, M.A., Tang, S., Draeger, D., Nambeesan, S., Shaffer, H., Barb, J.B., Knapp, S.J., Burke, J.M.: Genetic analysis of floral symmetry in Van Gogh’s sunflowers reveals independent recruitment of CYCLOIDEA genes in the Asteraceae. - PLoS Genet 8: e1002628, 2012.
Citerne, H.L., Le Guilloux, M., Sannier, J., Nadot, S., Damerval, C.: Combining phylogenetic and syntenic analyses for understanding the evolution of TCP ECE genes in Eudicots. - PLoS ONE 8: e74803, 2013.
Comai, L., Madlung, A., Josefsson, C., Tyagi, A.: Do the different parental’ heteromes’ cause genomic shock in newly formed allopolyploids? - Phil. Trans. roy. Soc. London B Biol. Sci. 358: 1149–1155, 2003.
Costa, M.M.R., Fox, S., Hana, A.I., Baxter, C., Coen, E.: Evolution of regulatory interactions controlling floral asymmetry. - Development 132: 5093–5101, 2005.
Cubas, P., Lauter, N., Doebley, J., Coen, E.: The TCP domain: a motif found in proteins regulating plant growth and development. - Plant J. 18: 215–222, 1999.
Damerval, C., Le Guilloux, M., Jager, M., Charon, C.: Diversity and evolution of CYCLOIDEA-like TCP genes in relation to flower development in Papaveraceae. - Plant Physiol 143: 759–772, 2007.
Dong, Z.Y., Wang, Y.M., Zhang, Z.J., Shen, Y., Lin, X.Y., Ou, X.F., Han, F.P., Liu, B.: Extent and pattern of DNA methylation alteration in rice lines derived from introgressive hybridization of rice and Zizania latifolia Griseb. - Theor. appl. Genet. 113: 196–205, 2006.
Eisses, J.F., Lafoe, D., Scott, L.A., Weil, C.F.: Novel, developmentally specific control of Ds transposition in maize. - Mol. gen. Genet. 256: 158–168, 1997.
Emmons, S.W., Yesner, L.: High-frequency excision of transposable element Tc1 in the nematode Caenorhabditis elegans is limited to somatic cells. - Cell 36: 599–605, 1984.
Esnault, C., Palavasam, A., Pilitt, K., O’Brochta, D.A.: Intrinsic characteristics of neighboring DNA modulate transposable element activity in Drosophila melanogaster. - Genetics 187: 319–331, 2011.
Fambrini, M., Basile, A., Salvini, M., Pugliesi, C.: Excisions of a defective transposable CACTA element (Tetu1) generate new alleles of a CYCLOIDEA-like gene of Helianthus annuus. - Gene 549: 198–207, 2014a.
Fambrini, M., Michelotti, V., Pugliesi, C.: The unstable tubular ray flower allele of sunflower: inheritance of reversion to wild type. - Plant Breed. 126: 548–550, 2007.
Fambrini, M., Salvini, M., Basile, A., Pugliesi, C.: Transposondependent induction of Vincent van Gogh’s sunflowers: exceptions revealed. - Genesis 52: 315–327, 2014b.
Fambrini, M., Salvini, M., Pugliesi, C.: A transposon-mediate inactivation of a CYCLOIDEA-like gene originates polysymmetric and androgynous ray flowers in Helianthus annuus. - Genetica 139: 1521–1529, 2011.
Fedoroff, N.V., Banks, J.A.: Is the Suppressor-mutator element controlled by a basic developmental regulatory mechanism? - Genetics 120: 559–577, 1988.
Feschotte, C., Pritham, E.J.: DNA-transposons and the evolution of eukaryotic genomes. - Annu. Rev. Genet. 41: 331–368, 2007.
García Guerreiro, M.P.: What makes transposable elements move in the Drosophila genome? - Heredity 108: 461–468, 2012.
Giedt, C.D., Weil, C.F.: The maize LAG1-0 mutant suggests that reproductive cell lineages show unique gene expression patterns early in vegetative development. - Plant J. 24: 815–823, 2000.
Gill, N., Buti, M., Kane, N., Bellec, A., Helmstetter, N., Berges, H., Rieseberg, L.K.: Sequence-based analysis of structural organization and composition of the cultivated sunflower (Helianthus annuus L.) genome. - Biology 3: 295–319, 2014.
Giordani, T., Cavallini, A., Natali, L.: The repetitive component of the sunflower genome. - Curr. Sci. Plant Biol. 1: 45–54, 2014.
Groose, R.W., Weigelt, H.D., Palmer, R.G.: Somatic analysis of an unstable mutation for anthocyanin pigmentation in soybean. - J. Heredity 79: 263–267, 1988.
Juntheikki-Palovaara, I., Tähtiharju, S., Lan, T., Broholm, S.K., Rijpkema, A.S., Ruonala, R., Kale, L., Albert, V.A., Teeri, T.H., Elomaa, P.: Functional diversification of duplicated CYC2 clade genes in regulation of inflorescence development in Gerbera hybrida (Asteraceae). - Plant J. 79: 783–796, 2014.
Laski, F.A., Rubin, G.M.: Analysis of the cis-acting requirements for germ-line specific splicing of the P-element ORF2-ORF3 intron. - Genes Dev. 3: 720–728, 1989.
Li, L.C., Dahiya R.: MethPrimer: designing primers for methylation PCRs. - Bioinformatics 18: 1427–1431, 2002.
Li, S.: The Arabidopsis thaliana TCP transcription factors: a broadening horizon beyond development. - Plant Signal. Behav. 10: e1044192, 2015.
Lisch, D.: How important are transposons for plant evolution? - Nat. Rev. Genet. 14: 49–61, 2013.
Liu, D., Crawford, N.M.: Characterization of the germinal and somatic activity of the Arabidopsis transposable element Tag1. - Genetics 148: 1445–1456, 1998.
Liu, D., Wang, R., Galli, M., Crawford, N.M.: Somatic and germinal excision activities of the Arabidopsis transposon Tag1 are controlled by distinct regulatory sequences within Tag1. - Plant Cell 13: 1851–1863, 2001.
Luo, D., Carpenter, R., Copsey, L., Vincent, C., Clark, J., Coen, E.S.: Control of organ asymmetry in flowers of Antirrhinum. - Cell 99: 367–376, 1999.
Luo, D., Carpenter, R., Vincent, C., Copsey, L., Coen, E.: Origin of floral asymmetry in Antirrhinum. - Nature 383: 794–799, 1996.
Luo, D., Coen, E.S., Doyle, S., Carpenter, R.: Pigmentation mutants produced by transposon mutagenesis in Antirrhinum majus. - Plant J. 1: 59–69, 1991.
Martín-Trillo, M., Cubas, P.: TCP genes: a family snapshot ten years later. - Trends Plant Sci. 15: 31–39, 2010.
McClintock, B.: The Suppressor-mutator system of control of gene action. - Carnegie Inst Wash Year Book 57: 415–429, 1958.
McClintock, B.: Further studies of the Suppressor-mutator system of control of gene action in maize. - Carnegie Inst Wash Year Book 60: 469–476, 1961.
Michalak, P.: Epigenetic, transposon and small RNA determinants of hybrid dysfunctions. - Heredity 102: 45–50, 2009.
Mizzotti, C., Fambrini, M., Caporali, E., Masiero, S., Pugliesi, C.: A CYCLOIDEA-like gene mutation in sunflower determines an unusual floret type able to produce filled achenes at the periphery of the pseudanthium. - Botany 93: 171–181, 2015.
Oliver, K.R., McComb, J.A., Greene, W.K.: Transposable elements: powerful contributors to angiosperm evolution and diversity. - Genome Biol. Evol. 5: 1886–1901, 2013.
Palmer, R.G., Hedges, B.R., Benavente, R.S., Groose, R.V.: w4- mutable line in soybean. - Dev. Genet. 10: 542–551, 1989.
Petit, M., Guidat, C., Daniel, J., Denis, E., Montoriol, E., Bui, Q.T., Lim, K.Y., Kovarik, A., Leitch, A.R., Grandbastien, M.-A., Mhiri, C.: Mobilization of retrotransposons in synthetic allotetraploid tobacco. - New Phytol. 186: 135–147, 2010.
Preston, J.C., Hileman, L.C.: Developmental genetics of floral symmetry evolution. - Trends Plant Sci. 14: 147–154, 2009.
Roccaro, M., Li, Y., Sommer, H.: ROSINA (RSI) is a part of a CACTA transposable element, TamRSI, and links flower development to transposon activity. - Mol. gen. Genomics 278: 243–254, 2007.
Sarilar, V., Martinez Palacios, P., Rousselet, A., Ridel, C., Falque, M., Eber, F., Chèvre, A.-M., Joets, J., Brabant, P., Alix, K.: Allopolyploidy has a moderate impact on restructuring at three contrasting transposable element insertion sites in resynthesized Brassica napus allotetraploids. - New Phytol. 198: 593–604, 2013.
Schläppy, M., Smith, D., Fedoroff, N.: TnpA trans-activates methylated maize Suppressor-mutator transposable elements in transgenic tobacco. - Genetics 133: 1009–1021, 1993.
Staton, S.E., Bakken, B.H., Blackman, B.K., Chapman, M.A., Kane, N.C., Tang, S., Ungerer, M.C., Knapp, S.J., Rieseberg, L.H., Burke, J.M.: The sunflower (Helianthus annuus L.) genome reflects a recent history of biased accumulation of transposable elements. - Plant J. 72: 142–153, 2012.
Tähtiharju, S., Rijpkema, A.S., Vetterli, A., Albert, V.A., Teeri, T.H., Elomaa, P.: Evolution and diversification of the CYC/TB1 gene family in Asteraceae–a comparative study in gerbera (Mutisieae) and sunflower (Heliantheae). - Mol. Biol. Evol. 29: 1155–1166, 2012.
Thompson, J.D., Higgins, D.G., Gibson, T.J.: CLUSTALW: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. - Nucl. Acids Res. 22: 4673–4680, 1994.
Uberti Monassero, N.G., Viola, I.L., Welchen, E., Gonzalez, D.H.: TCP transcription factors: architectures of plant form. - Biomol. Concepts 4: 111–127, 2013.
Ungerer, M.C., Strakosh, S.C., Zhen, Y.: Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation. - Curr. Biol. 16: R872–R873, 2006.
Verhoeven, K.J.F., Van Dijk, P.J., Biere, A.: Changes in genomic methylation patterns during the formation of triploid asexual dandelium lineages. - Mol. Ecol. 19: 315–324, 2010.
Vukich, M., Giordani, T., Natali, L., Cavallini, A.: Copia and Gypsy retrotransposons activity in sunflower (Helianthus annuus L.). - BMC Plant Biol. 23: 9150, 2009a.
Vukich, M., Schulman, A.H., Giordani, T., Natali, L., Kalendar, R., Cavallini, A.: Genetic variability in sunflower (Helianthus annuus L.) and in the Helianthus genus as assessed by retrotransposon-based molecular markers. - Theor. appl. Genet. 119: 1027–1038, 2009b.
Wang, J., Tian, L., Lee, H.S., Wei, N.E., Jiang, H., Watson, B., Madlung, A., Osborn T.C., Doerge, R.W., Comai, L., Chen, Z.J.: Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. - Genetics 172: 507–517, 2006.
Wang, Z., Luo, Y.H., Li, X., Wang, L.P., Xu, S.L., Yang, J., Weng, L., Sato, S.S., Tabata, S., Ambrose, M., Rameau, C., Feng, X.Z., Hu, X.H., Luo, D.: Genetic control of floral zygomorphy in pea (Pisum sativum L.). - Proc. nat. Acad. Sci. USA 105: 10414–10419, 2008.
Wicker, T., Guyot, R., Yahiaoui, N., Keller, B.: CACTA transposons in Triticeae. A diverse family of high-copy repetitive elements. - Plant Physiol. 132: 52–63, 2003.
Xu, M., Brar, H.K., Grosic, S., Palmer, R.G., Bhattacharyya, K.: Excision of an active CACTA-like transposable element from DFR2 causes variegated flowers in soybean [Glycine max (L.) Merr.]. - Genetics 153: 53–63, 2010.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Fambrini, M., Pugliesi, C. Mobilization of the Tetu1 transposable element of Helianthus annuus: evidence for excision in different developmental stages. Biol Plant 61, 55–63 (2017). https://doi.org/10.1007/s10535-016-0655-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10535-016-0655-x